In Situ Optical Feedback in Brain Tumor Biopsy: A Multiparametric Analysis

Overview

Journal Neurooncol Adv

Publisher Oxford University Press

Date 2024 Dec 17

PMID 39687792

Authors

Elisabeth Klint

Johan Richter

Peter Milos

Martin Hallbeck

Karin Wardell

Affiliations

Soon will be listed here.

Abstract

Background: Brain tumor needle biopsy interventions are inflicted with nondiagnostic or biased sampling in up to 25% and hemorrhage, including asymptomatic cases, in up to 60%. To identify diagnostic tissue and sites with increased microcirculation, intraoperative optical techniques have been suggested. The aim of this study was to investigate the clinical implications of in situ optical guidance in frameless navigated tumor biopsies.

Methods: Real-time feedback on protoporphyrin IX (PpIX) fluorescence, microcirculation, and gray-whiteness was given before tissue sampling (272 positions) in 20 patients along 21 trajectories in total. The primary variables of investigation were fluorescence in relation to neuropathological findings and gadolinium (Gd) enhancement, increased cerebral microcirculation in relation to bleeding incidence, number of trajectories, and impact on operation time.

Results: PpIX fluorescence was detected in Glioblastoma IDH-wildtype CNS WHO grade 4 ( = 12), Primary diffuse large B-cell lymphoma ( = 3), astrocytoma IDH-mutated CNS WHO grade 4 ( = 1) (Ki67 indices ≥ 15%). For 2 patients, no PpIX fluorescence or Gd was found, although samples contained tumorous tissue (Ki67 index 6%). Increased microcirculation was found along 9 trajectories (34 sites), located in cortical, tumorous, or tentorium regions. Postoperative bleedings ( = 10, nine asymptomatic) were related to skull opening or tissue sampling. This study strengthens the proposed independence from intraoperative neuropathology as PpIX fluorescence is detected. Objective real-time feedback resulted in fewer trajectories compared to previous studies indicating reduced operation time.

Conclusions: The integrated optical guidance system provides real-time feedback in situ, increasing certainty and precision of diagnostic tissue before sampling during frameless brain tumor biopsies.

References

Suero Molina E, Black D, Walke A, Azemi G, DAlessandro F, Konig S . Unraveling the blue shift in porphyrin fluorescence in glioma: The 620 nm peak and its potential significance in tumor biology. Front Neurosci. 2023; 17:1261679. PMC: 10657867. DOI: 10.3389/fnins.2023.1261679. View

von Campe G, Moschopulos M, Hefti M . 5-Aminolevulinic acid-induced protoporphyrin IX fluorescence as immediate intraoperative indicator to improve the safety of malignant or high-grade brain tumor diagnosis in frameless stereotactic biopsies. Acta Neurochir (Wien). 2012; 154(4):585-8. PMC: 3308005. DOI: 10.1007/s00701-012-1290-8. View

Klint E, Mauritzon S, Ragnemalm B, Richter J, Wardell K . FluoRa - a System for Combined Fluorescence and Microcirculation Measurements in Brain Tumor Surgery. Annu Int Conf IEEE Eng Med Biol Soc. 2021; 2021:1512-1515. DOI: 10.1109/EMBC46164.2021.9629801. View

Klint E, Richter J, Wardell K . Combined Use of Frameless Neuronavigation and In Situ Optical Guidance in Brain Tumor Needle Biopsies. Brain Sci. 2023; 13(5). PMC: 10216526. DOI: 10.3390/brainsci13050809. View

Richter J, Haj-Hosseini N, Hallbeck M, Wardell K . Combination of hand-held probe and microscopy for fluorescence guided surgery in the brain tumor marginal zone. Photodiagnosis Photodyn Ther. 2017; 18:185-192. DOI: 10.1016/j.pdpdt.2017.01.188. View

Jaber M, Wolfer J, Ewelt C, Holling M, Hasselblatt M, Niederstadt T . The Value of 5-Aminolevulinic Acid in Low-grade Gliomas and High-grade Gliomas Lacking Glioblastoma Imaging Features: An Analysis Based on Fluorescence, Magnetic Resonance Imaging, 18F-Fluoroethyl Tyrosine Positron Emission Tomography, and Tumor.... Neurosurgery. 2015; 78(3):401-11. PMC: 4747980. DOI: 10.1227/NEU.0000000000001020. View

Riche M, Amelot A, Peyre M, Capelle L, Carpentier A, Mathon B . Complications after frame-based stereotactic brain biopsy: a systematic review. Neurosurg Rev. 2020; 44(1):301-307. DOI: 10.1007/s10143-019-01234-w. View

Louis D, Perry A, Wesseling P, Brat D, Cree I, Figarella-Branger D . The 2021 WHO Classification of Tumors of the Central Nervous System: a summary. Neuro Oncol. 2021; 23(8):1231-1251. PMC: 8328013. DOI: 10.1093/neuonc/noab106. View

Rejmstad P, Akesson G, Aneman O, Wardell K . A laser Doppler system for monitoring cerebral microcirculation: implementation and evaluation during neurosurgery. Med Biol Eng Comput. 2015; 54(1):123-31. DOI: 10.1007/s11517-015-1332-5. View

10.

Livermore L, Ma R, Bojanic S, Pereira E . Yield and complications of frame-based and frameless stereotactic brain biopsy--the value of intra-operative histological analysis. Br J Neurosurg. 2014; 28(5):637-44. DOI: 10.3109/02688697.2014.887657. View

11.

Mehidine H, Chalumeau A, Poulon F, Jamme F, Varlet P, Devaux B . Optical Signatures Derived From Deep UV to NIR Excitation Discriminates Healthy Samples From Low and High Grades Glioma. Sci Rep. 2019; 9(1):8786. PMC: 6584506. DOI: 10.1038/s41598-019-45181-4. View

12.

Evers G, Kamp M, Warneke N, Berdel W, Sabel M, Stummer W . 5-Aminolaevulinic Acid-Induced Fluorescence in Primary Central Nervous System Lymphoma. World Neurosurg. 2016; 98:375-380. DOI: 10.1016/j.wneu.2016.11.011. View

13.

Zsigmond P, Hemm-Ode S, Wardell K . Optical Measurements during Deep Brain Stimulation Lead Implantation: Safety Aspects. Stereotact Funct Neurosurg. 2018; 95(6):392-399. DOI: 10.1159/000484944. View

14.

Wardell K, Klint E, Milos P, Richter J . One-Insertion Stereotactic Brain Biopsy Using In Vivo Optical Guidance-A Case Study. Oper Neurosurg (Hagerstown). 2023; 25(2):176-182. PMC: 10313274. DOI: 10.1227/ons.0000000000000722. View

15.

Fontana A, Piffaretti D, Marchi F, Burgio F, Faia-Torres A, Paganetti P . Epithelial growth factor receptor expression influences 5-ALA induced glioblastoma fluorescence. J Neurooncol. 2017; 133(3):497-507. PMC: 5537329. DOI: 10.1007/s11060-017-2474-0. View

16.

Qian Z, Victor S, Gu Y, Giller C, Liu H . Look-Ahead Distance of a fiber probe used to assist neurosurgery: Phantom and Monte Carlo study. Opt Express. 2009; 11(16):1844-55. DOI: 10.1364/oe.11.001844. View

17.

Shofty B, Richetta C, Haim O, Kashanian A, Gurevich A, Grossman R . 5-ALA-assisted stereotactic brain tumor biopsy improve diagnostic yield. Eur J Surg Oncol. 2019; 45(12):2375-2378. DOI: 10.1016/j.ejso.2019.07.001. View

18.

Alston L, Mahieu-Williame L, Hebert M, Kantapareddy P, Meyronet D, Rousseau D . Spectral complexity of 5-ALA induced PpIX fluorescence in guided surgery: a clinical study towards the discrimination of healthy tissue and margin boundaries in high and low grade gliomas. Biomed Opt Express. 2019; 10(5):2478-2492. PMC: 6524587. DOI: 10.1364/BOE.10.002478. View

19.

Valdes P, Kim A, Brantsch M, Niu C, Moses Z, Tosteson T . δ-aminolevulinic acid-induced protoporphyrin IX concentration correlates with histopathologic markers of malignancy in human gliomas: the need for quantitative fluorescence-guided resection to identify regions of increasing malignancy. Neuro Oncol. 2011; 13(8):846-56. PMC: 3145475. DOI: 10.1093/neuonc/nor086. View

20.

Boden A, Molin J, Garvin S, West R, Lundstrom C, Treanor D . The human-in-the-loop: an evaluation of pathologists' interaction with artificial intelligence in clinical practice. Histopathology. 2021; 79(2):210-218. DOI: 10.1111/his.14356. View